MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 256: 171–182, 2003 Published July 17

INTRODUCTION

Related groups of animals can vary greatly in themorphology of certain characters. A possible causeof these variations is the interaction between preda-tors and prey, since predation is an important selec-tive force affecting the fitness of all individuals inprey populations (Edmunds 1974, Harvey & Green-wood 1978, Sih 1987, Vermeij 1987). Predators affectaspects of their prey beyond that of morphology: theyalso affect their prey’s chemistry, physiology, ecology,and behavior (e.g. Sih 1987), and cause the evolutionof a variety of defense traits which Janzen (1981)

argues are more diverse than any other array oftraits.

Defense traits were traditionally lumped togetherunder the heading of ‘antipredator characteristics’(Edmunds 1974, Vermeij 1982), and it was debatedwhether their evolution required that some prey sur-vived attacks (i.e. ‘unsuccessful’ or ‘incomplete’ preda-tion) (Vermeij 1982, 1985, Sih 1985). Subsequently, Sih(1987) and Brodie et al. (1991) divided antipredatorcharacteristics into 2 categories based on whether theyfunctioned before or after a predator detected its prey,i.e. predator-avoidance mechanisms and antipredatormechanisms. Predator-avoidance mechanisms enable

© Inter-Research 2003 · www.int-res.com*Email: barshaw@ocean.org.il

Offense versus defense: responses of three morphological types of lobsters to predation

Diana E. Barshaw1, 4,*, Kari L. Lavalli1, 3, Ehud Spanier1, 2

1Leon Recanati Institute for Maritime Studies, and 2Department for Maritime Civilizations, University of Haifa, Mount Carmel, Haifa 31905, Israel

3The Lobster Conservancy, PO Box 235, Friendship, Maine 04547, USA

4Present address: Israel Oceanographic & Limnological Research Institute, PO Box 8030, Haifa 31080, Israel

ABSTRACT: We compared the antipredator mechanisms of 3 morphological ‘types’ of lobsters: slip-per lobsters Scyllarides latus, spiny lobsters Palinurus elephas and clawed lobsters Homarus gam-marus. These lobsters differ in the extent and effectiveness of their weaponry and armor, which weassessed by: (1) field tethering experiments that compared relative survival of intact and manipulated(clinging ability, antennae, or claws removed) lobsters in the face of predation, and (2) measurementsof the breaking strength and thickness of the carapace of each species. Intact clawed lobsterssuffered higher mortality than either intact slipper or spiny lobsters after both 4 and 24 h. At 24 h,intact spiny lobsters also had higher mortality than intact and manipulated slipper lobsters. The intactspiny and clawed lobsters suffered less predation after 4 h than the manipulated lobsters (lackingweapons); however, this advantage diminished or vanished by 24 h. This indicates that weapons pro-vided some measure of protection in the short-term, which might be sufficient to allow the lobsters toescape from a predator using a strong abdominal tail flip. Triggerfish Balistes carolinensis were theprimary predators on the lobsters. We also saw octopuses Octopus vulgaris feeding on lobsters, butthese were never observed subduing a live lobster. ‘Punch’-tests (i.e. puncture tests) on the carapacesof each of the 3 species showed that slipper lobsters had stronger armor than either spiny or clawedlobsters, while the spiny lobster armor was intermediate in strength. These results suggest that thedefensive strong armor of slipper lobsters is a more effective antipredatory mechanism than theoffensive morphological weapons of the spiny and clawed lobsters.

KEY WORDS: Predator-prey interactions · Predator-avoidance · Antipredator mechanisms · Weapons ·Armor · Lobsters · Scyllarides latus · Palinurus elephas · Homarus gammarus

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 256: 171–182, 2003

prey to avoid predation by being active at times whentheir predators are not active (temporal avoidance), byblending into the background (crypsis), by livingwhere the predators cannot (spatial avoidance), byavoiding notice (immobility), or by sheltering, burying,or reducing general activity levels (slow lifestyle) (Sih1987, Brodie et al. 1991). These strategies prevent orreduce the likelihood of encounters with predators. Incontrast, antipredator mechanisms increase the proba-bility of survival once detected. They include flight,unpredictable movements or changes in form or color(protean behavior), armor, weaponry, distastefulness,venom, and aggregation (Herrnkind et al. 1975, 2001,Endler 1986, Sih 1987, Driver & Humphries 1988,Lavalli & Spanier 2001). Sih (1987) argued that theselective pressures resulting in the evolution of these2 mechanisms differ: predator avoidance mechanismscan evolve in cases of complete predation, i.e. whenthe prey never survive an attack: those prey that neverencounter a predator because of their avoidance mech-anisms survive to reproduce and reinforce the avoid-ance mechanisms. On the other hand, antipredatormechanisms evolve only in the case of unsuccessfulpredation, whereby prey use an antipredator mecha-nism to escape and later reproduce (Vermeij 1982,Brodie et al. 1991). Predator-avoidance mechanismsand antipredator mechanisms are, therefore, distinct.

Crustaceans lend themselves to in-depth studies onthe evolution of antipredator mechanisms becausetheir morphological weaponry usually comprises mod-ified appendages that can be removed by autotomywith few short-term effects. In the long-term, limbautotomy can impact the ability of crustaceans to feed,grow, and to find mates (Juanes & Hartwick 1990,Smith 1992), but such long-term effects have littlerelevance for short-term experiments.

For our investigation on the variations in antipredatormechanisms between related groups, we chose speciesrepresentative of the 3 major families of lobster: Scyllar-idae, Palinuridae, and Nephropidae. These 3 co-occurthroughout most of their ranges in the eastern AtlanticOcean and Mediterranean Sea (Maigret 1978, Fisheret al. 1981, Martins 1985, Williams 1988, Holthuis 1991)(Fig. 1). The slipper lobster Scyllarides latus is found atdepths of 4 to 100 m, usually on rocky or sandy bottoms.S. latus bears no spines on its flattened carapace, havingnumerous blunt tubercules instead, and has reduced,shovel-like, flat second antennae. This lobster is capableof retracting its small eyes into sunken orbits (Phillips etal. 1980). The common spiny lobster Palinurus elephas isfound at depths of 5 to 160 m, usually on rocky bottoms.Like all other spiny lobsters, it bears sharp spines alongthe dorsal surface of its carapace and on its long, broad,whip-like second antennae. It has horns protecting itslarge, stalked eyes (Holthuis 1991, Hunter 1999). The

European clawed lobster, Homarus gammarus, is foundat depths of 0 to 150 m on rocky substrates. Its first walk-ing legs are modified into large claws of unequal size. Itscarapace is smooth, with few spines, and it has stalkedeyes with no protection.

We compared: (1) the actual effectiveness of thepresumed antipredator mechanism of each species,

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Fig. 1. (a) Scyllarides latus, (b) Palinurus elephas and (c)Homarus gammarus. Geographic range (horizontal line-

shading) of the 3 lobster species studied

(a)

(c)

(b)

Barshaw et al.: Offense vs defense in lobsters

(2) which morphological type of lobster fared betteragainst predation, and (3) the actual strength andthickness of the carapace of each species.

MATERIALS AND METHODS

Lobsters. Slipper lobsters were purchased from localfisherman in Haifa, Israel. Spiny and clawed lobsterswere purchased from suppliers in Colchester, England,and Galway, Ireland, and shipped to us in coolers byairfreight. On arrival, they were gradually acclimatedto local water conditions. The lobsters were allowed tocompletely recuperate from any handling effects for atleast 4 wk. They were held communally (separated byspecies) in tanks with shelters and flow-through, am-bient, unfiltered seawater. All the lobsters were fedad libitum on a variety of local molluscs, including thebivalves Pinctata radiata and Spondylus spinosus, thelimpets Patella caerulea and snails Monodonta turbi-nata. All lobsters used were mature specimens, rang-ing in size from 73 to 158 mm carapace length (CL).

Each of the 3 species was used in 2 configurations:(1) intact, and (2) manipulated, whereby a particular(suspected) antipredator mechanism was removed(Fig. 2). Manipulations of spiny and clawed lobsters weremade by pinching the autotomy joints with needle-nosed pliers and forcing the lobster to drop eitherits claw or its antennae. Lobsters already lacking 1 ofthese appendages were purchased from commercialagents, making autotomy of only 1 limb necessary.Slipper lobsters were manipulated by having theirwalking legs bound with wire ties. Thus manipulatedslipper lobsters could not cling to the substrate, manip-

ulated spiny lobsters had no second antennae, andmanipulated clawed lobsters had no claws. Autotomyof appendages is a natural ability in crustaceans, andforced autotomy did not cause any mortality or sick-ness during these experiments.

Study site. We drove 30 iron stakes into a relativelyfeatureless, bare area composed of biogenic rock par-tially covered with seasonal patches of the alga Padinagymnospora. The stakes were arranged into a circle of12 m radius, with each stake 2.5 m apart. Each stakewas numbered with a white plastic tag and stoodapproximately 30 cm above the substrate. The circlewas located 30 m from artificial tire reefs 1700 m south-west of Tel Shikmona, Haifa, Israel, at a depth of18.5 m. This site is known to harbor many fish speciesincluding the moray eel, wrasses, sparids, groupersEpinephelus marginatus, E. alexandrinus, and trigger-fish Balistes carolinensis, as well as the commonoctopus Octopus vulgaris (Spanier et al. 1990).

Predation experiments. Previous field experiments(Barshaw & Spanier 1994a) have shown that predationpressure increases to a maximum over time as thepredators in an area alert to an increase in availableprey (typical Type II or III numerical response to preydensity whereby predation levels off: Holling 1959). Aswe wished to maintain a constant predation pressure,we baited the field site with fresh and frozen bluecrabs and with dead frozen specimens of the 3 lobsterspecies for 3 wk prior to experiments. In this way, weavoided a lower predation rate during the first fewruns of the experiment.

We examined 30 lobsters (10 of each species; 5 in-tact, 5 manipulated) for injuries or missing appendages.We then sexed them, and measured them prior to

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Fig. 2. Scyllarides latus, Palinurus elephas and Homarus gammarus. Line drawings of the 3 lobster species. M: manipulation per-formed on the respective species (manipulation was on both sides of each lobster, not only on 1 side as shown here). BACK, BE(between eyes, anterior to gastric chamber), SIDE: points on carapace that were punctured using MTS servo-controlled,

hydraulic testing machine. (Modified from diagrams of P. Bernucci in: Falciai & Minervini 1992)

Mar Ecol Prog Ser 256: 171–182, 2003

tethering. After tethering, the lobsters were assignedto particular stakes, and taken to the field site. Alllobsters were tethered to stakes in the field by two 1 mlong, 50 kg test monofilament lines knotted and super-glued to a black wire tie that was placed around thecarapace of the lobsters behind the first 2 pairs of walk-ing legs, as described by Barshaw & Able (1990) andBarshaw & Spanier (1994a).

After tethering, the lobsters were observed bySCUBA divers, and their behavior while under attackwas recorded on videotape (SONY Handycam ProVideo Hi-8 3CCD-VXIE, RMT 702 camera in anAmphibico 3CCD Pro VX Series) for the first 40 minafter being tethered and again after 4 h. Lobster sur-vival was checked at 4 and 24 h. At 24 h, all survivinglobsters and remains were retrieved. We conducted4 runs from May to June 1996. Water temperaturesranged from 19 to 22°C (mean = 20.6°C) during thisperiod. A lobster was considered preyed upon only ifits carapace remains were found in the vicinity ofwhere it had been tethered. In this experiment, proba-bly because of our double-tether system, no lobsterescaped and all remains were recovered.

The number of lobsters that survived in the 4 runs ofthe experiment were initially tested by heterogeneitychi-square analysis (Zar 1996) to ensure that the runswere from the same population, which allowed them tobe pooled (4 h: χ2 = 8.99, p = 0.88; 24 h: χ2 = 22.2,p = 0.10). The pooled data were then organized in two3 × 2 × 2 contingency tables for 4 and 24 h (Table 1).These tables were analyzed using chi-square multi-dimensional contingency tables as demonstrated byFienberg (1970). The initial partof this analysis was also de-scribed by Zar (1996); however,he did not include the interac-tive method required to analyzefor interaction between factors.

The effects of size on the num-ber of lobsters that survived wasanalyzed using a 3-way ANOVA,where Factor A = species, FactorB = manipulation, and FactorC = survival.

Carapace strength. We con-ducted ‘punch’-tests on theshells of representatives of eachof the 3 lobster species tocompare the differences in thestrength of their carapaces.Lobsters were preserved byfreezing and then placed insealed plastic bags. Prior to test-ing, the lobsters were thawedand placed in an Inter Technol-

ogy MTS (Material Testing System) servo-controlled,hydraulic testing machine at the Materials Laboratoryin the Department of Engineering at the Technion Insti-tute for Technology in Haifa, Israel. This machine ap-plies increasing force onto a probe of certain diameterto eventually puncture the carapace of the animal be-ing tested. We chose a probe that approximated theshape, size, and sharpness of the mouth of a triggerfish(the main predator of the lobsters in our experiment).The shell of each individual lobster was tested in 3areas. Two of these areas represented typical points ofattack as noted in the field: Back (immediately posteriorto the dorsal cervical groove) and BE (between the eyesand anterior to the gastric chamber of the stomach).The third area tested was a less usual point attack: Side(along the branchial chambers on the side of the cara-pace just posterior to the cervical and hepatic grooves);Fig. 2 shows these locations for the 3 lobster species.We removed representative pieces of carapace fromthese same points, measured shell thickness (to0.01 mm) with calipers, and photographed details of theinternal carapace structure (Fig. 3). All lobsters wereexamined for molt condition at this time. Premolt andimmediately postmolt individuals were eliminated fromthe analysis, as their shells undergo changes in calci-fication at these molt stages.

The results were analyzed with 2 repeated-measuremultivariate analyses of variance (MANOVAs) fol-lowed by 18 pairwise comparisons using Student’st-tests. Repeated comparisons increase the probabilityof making a Type I error, so we applied the Bonferronicorrection at the α level.

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Table 1. Scyllarides latus, Palinurus elephas and Homarus gammarus. Null (H0) and al-ternate (Ha) hypothesis for each part of the 3 × 2 × 2 contingency tables, and the χ2 and

p-values for each, after 4 h and 24 h of predation

Factor Hypothesis

A: H0: Neither species of lobster nor manipulation has any effect on survival(mutually independent)

Ha: Either species of lobster, or manipulation has an effect on survival4 h: χ2 = 70.2 p < 0.000001 Reject H024 h: χ2 = 71.4 p < 0.000001 Reject H0

B: H0: Species of lobster, irrespective of manipulation, has no effect on survivalHa: Species of lobster, irrespective of manipulation, has an effect on survival4 h: χ2 = 58.8 p < 0.000001 Reject H024 h: χ2 = 69.5 p < 0.000001 Reject H0

C: H0: Manipulation of lobster, irrespective of species, has no effect on survivalHa: Manipulation of lobster, irrespective of species, has an effect on survival4 h: χ2 = 26.8 p = 0.00006 Reject H024 h: χ2 = 10.6 p = 0.06 Do not reject H0

D: H0: There is no interaction between species of lobster and manipulationHa: There is an interaction between species of lobster and manipulation4 h: χ2 = 8.98 p = 0.01 Reject H024 h: χ2 = 3.69 p = 0.16 Do not reject H0

Barshaw et al.: Offense vs defense in lobsters

Regression analysis determined therelationships between (1) shell thicknessand the force required to puncture it, and(2) size of the lobster and the forcerequired to puncture the shell.

RESULTS

Predation

Mortality after 4 h predation (Fig. 4a)

There was no significant difference inmortality between intact and manipulatedslipper lobsters. The manipulated spinyand clawed lobsters, however, displayedsignificantly higher mortality than theirintact conspecifics (Fig. 4a, Table 2).

Intact slipper lobsters and intact spiny lobsters hadsimilar mortality rates, but suffered significantly lowermortality than intact clawed lobsters. Manipulated slip-per lobsters, however, suffered significantly lower mor-tality than manipulated spiny and clawed lobsters, andboth manipulated slipper and spiny lobsters displayedsignificantly lower mortality than manipulated clawedlobsters, with the latter suffering 100% mortality.

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Fig. 3. Scyllarides latus, Palinurus elephas and Homarusgammarus. Photographs of parts of internal carapace of the3 species showing differences in structure. H. gammarus doesnot have deep pitting of shell, while S. latus and P. elephas do

0

20

40

60

80

100

120

Slipper Spiny ClawedP

erce

nt m

orta

lity

(%)

intact

manipulated

0

20

40

60

80

100

0

intact

manipulated

b

a

20 20

20

20

20

19

19

19

19

20

18

18

Fig. 4. Scyllarides latus, Palinurus elephas and Homarusgammarus. Percent mortality after (a) 4 h and (b) 24 h preda-tion. See Table 2 for pairwise comparisons. Error bars = SE;

numbers above bars = numbers of lobsters

Table 2. Scyllarides latus, Palinurus elephas and Homarus gammarus. χ2 andp-values from pairwise multiple comparisons (2 × 2 contingency tables) ofmortality between the 2 treatments and the 3 species after 4 and 24 h (Fig. 4). Sl: slipper lobster; Sp: spiny lobster; Cl: clawed lobster, ns: not significant

4 h mortality χ.2 . p 24 h mortality χ.2 . p

Intact vs manipulated Intact plus manipulatedSlipper 0.5 0.46 ns Cl vs Sp 7.1 0.008Spiny 12.8 0.0003 Cl vs Sl 55.9 <0.0001Clawed 8.7 0.0031 Sl vs Sp 28.4 <0.0001

IntactCl vs Sp 11.8 0.0006Cl vs Sl 9.4 0.0021Sl vs Sp 0.0007 0.98 ns

ManipulatedCl vs Sp 8.2 0.0042Cl vs Sl 32.5 <0.0001Sl vs Sp 10.4 0.0012

Mar Ecol Prog Ser 256: 171–182, 2003

Mortality after 24 h predation (Fig. 4b)

After 24 h, while species continued to have a signifi-cant effect on survival (Table 1B), manipulation was nolonger important. Therefore, the only pairwise com-parisons we could make were of survival differencesbetween species. Slipper lobsters suffered significantlyless predation than either spiny lobsters or clawedlobsters, and spiny lobsters suffered significantly lesspredation than clawed lobsters (Fig. 4b, Table 2).

Size (Fig. 5)

Among the 3 species (F = 17.8, p < 0.001), spiny lob-sters were significantly larger than clawed (F = 3.589,p < 0.05) and slipper (F = 3.846, p < 0.05) lobsters. After24 h, surviving intact spiny lobsters were larger thanthose spiny lobsters that had been eaten (F = 4.508,p < 0.05).

Predation observations

We observed and recorded predation in all 4 runs ofthis experiment. The predators consisted mainly ofgroups of 4 to 11 gray triggerfish Balistes carolinensis (asynonym of B. capriscus, pers. comm. of A. Ben-Tuvia,Hebrew University, Jerusalem). Octopuses were twiceseen eating clawless Homarus gammarus, but the

lobsters were already dead when these observationstook place. We never saw an octopus subdue a lobster.

In a typical attack sequence against slipper lobsters,the triggerfish would approach the lobster severaltimes without actually striking (see Lavalli & Spanier2001 for diagramatic sequence of triggerfish attack onslipper lobsters). During these passes, the fish wouldchange from vertical to horizontal swimming, andwould seem to ‘blow’ at the lobster. The slipper lob-sters did not move during these passes. The fish wouldthen strike at the lobster; even after such a strike, theslipper lobster would often not move. Finally, the fishwould manage to take a bite out of the lobster, oftenfrom the flattened second antennae, which wouldcause the slipper lobster to tail-flip explosively (to theextent of its tether). Once during this experiment, andtwice in preliminary experiments, this sudden move-ment on the part of a slipper lobster startled the attack-ing fish and stopped further attacks for several min-utes. Eventually the fish would subdue the lobster bycatching it during a tail-flip, turning it over on its back,biting off 1 or more legs, and finally biting through theventral sternal plates, as described previously by Bar-shaw & Spanier (1994a). The most consistent part ofthis sequence of behavior was the complete immobilityof the slipper lobsters during the first part of the attack.

This behavior of the slipper lobsters differedmarkedly from the behavior of both spiny and clawedlobsters. Spiny and clawed lobsters would alert to thepresence of the fish by turning and facing theirattacker. These lobsters always tried to keep theirrespective weapons (long spiny antennae or claws)facing the fish. Spiny lobsters would fend the fish offwith their antennae by pointing or trapping it betweenthe 2 antennae, where they could whip and lunge atthe fish to scrape or scratch it (for QuickTime movies ofspiny lobster defense behavior against triggerfish seehttp://bio.fsu.edu/~herrnlab/cooperativedefense.html).Clawed lobsters mainly used their claws to fend off anattacking fish by jabbing, but they also occasionallysnapped at the fish. The strategy of the triggerfish inall these maneuvers was to bite off the eyestalks or dis-able the weapons of the lobsters. To do this, the fishwould either attempt to dart in behind the lobster awayfrom its weapons, or would take bites out of the anten-nae or the claws until these were rendered less effec-tive as weapons. If the fish did remove a lobster’s eyes,then the lobster was no longer able to maintain its posi-tion in reference to the fish. At that point, the clawedlobsters were killed with 1 quick bite through theirdorsal carapace. Several attacks were required tobreak through the carapace of spiny lobsters. The mostconsistent part of this sequence of behavior was theattempt by the lobsters to position themselves withtheir weapons facing the predator.

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Fig. 5. Scyllarides latus, Palinurus elephas and Homarusgammarus. Mean carapace length (CL) of lobsters eaten andnot eaten during field predation experiment. Error bars = SE;numbers above bars = numbers of lobsters; Int.: intact; Man.:

manipulated; ne: not eaten

Barshaw et al.: Offense vs defense in lobsters

Carapace strength

Puncture tests (Fig. 6a)

There were significant differences in the force re-quired to puncture the carapaces of the 3 lobster spe-cies (F = 67.07, p < 0.0001). Significantly more force, upto 3 times as much (paired t-test with Bonferroni cor-rection; see Table 3 for all p-values), was required topuncture the carapace of slipper lobsters compared tothat of spiny or clawed lobsters at all 3 points on thecarapace. At Point Back, significantly more force wasrequired to puncture the carapace of spiny lobstersthan to puncture the carapace of clawed lobsters. Therewas no significant difference between the carapace ofspiny and clawed lobsters at either Point BE or Side.

Comparing the 3 different locations on the carapacewithin groups, there was a significant difference in theforce required to puncture the carapace at the 3 differ-ent points (F = 52.1, p < 0.0001). In slipper lobsters,Points Back and BE were not significantly different,but they were both significantly stronger than PointSide. In spiny lobsters, Point Back was stronger thanPoint BE, which was stronger than Point Side. Amongclawed lobsters, there was no significant differencein the strength of the carapace between the 3 points.

There was a significant interaction between speciesand location of the puncture test, since the strongest pointon the carapace differed as a function of species (betweenspecies × repeated measure, F = 11.4, p = 0.0001).

Carapace thickness (Fig. 6b)

Among the 3 lobster species, there was a significantdifference in the thickness of the carapace (F = 262.0,p < 0.0001). The carapace of slipper lobsters was sig-nificantly thicker (up to twice as thick) as that of spinyor clawed lobsters for all 3 points on the carapace. AtPoint Back, the spiny lobsters’ carapace was thickerthan that of the clawed lobsters; otherwise there wereno significant differences.

Comparing the 3 different locations on the carapacewithin a species, there was a significant difference in thethickness of the carapace at the different points (F = 19.9,p = 0.0001). The only significant difference among slip-per lobsters was that Point Back was thicker than PointBE. The only significant difference among spiny lobsterswas that Point BE was thicker than Point Side. Amongclawed lobsters, there was no significant difference inthe thickness of the carapace between the 3 points.

There was a significant interaction between speciesand the location of the puncture test, since the thickestpoint on the carapace differed as a function of species(between species × repeated measure: F = 12.8, p = 0.0001).

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Fig. 6. Scyllarides latus, Palinurus elephas and Homarusgammarus. (a) Mean force required to puncture carapace; (b)mean thickness of carapace. See Table 3 for pairwise compar-isons and Fig. 2 for positions of the 3 puncture points. Errorbars = SE; 14 slipper, 20 clawed and 18 spiny lobsters were

used for measurements

Table 3. Scyllarides latus, Palinurus elephas and Homarusgammarus. t and p values from pairwise comparisons (Stu-dent’s t-test) of force required to puncture carapace of the 3species at 3 designated points (Fig. 6a) and of thickness ofcarapace at the 3 designated points (Fig. 6b). BE: betweeneyes; Sl: slipper lobster; Sp: spiny lobster; Cl: clawed lobster.Bonferroni correction indicated that only when p < 0.0028

were the results significant

Comparison Force Thicknesst p t p

Slipper lobstersBack vs Side 6.0 <0.001 2.2 nsBE vs Back 0.03 ns 4.2 <0.001BE vs Side 4.7 <0.001 2.5 ns

Spiny lobstersBack vs Side 6.7 <0.001 4.2 <0.001BE vs Back 5.1 <0.001 3.6 nsBE vs Side 5.4 <0.001 1.9 ns

Clawed lobstersBack vs Side 1.5 ns 1.4 nsBE vs Back 3.2 ns 2.4 nsBE vs Side 3.6 ns 3.4 ns

BackSl vs Cl 13.80 <0.001 21.00 <0.001Sl vs Sp 4.9 <0.001 15.10 <0.001Sp vs Cl 5.3 <0.001 3.3 <0.002

BESl vs Cl 11.40 <0.001 16.90 <0.001Sl vs Sp 6.4 <0.001 12.80 <0.001Sp vs Cl 3.0 ns 0.3 ns

SideSl vs Cl 12.20 <0.001 26.00 <0.001Sl vs Sp 8.1 <0.001 18.40 <0.001Sp vs Cl 2.8 ns 0.030 ns

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Regressions

There was no significant relationship between lob-ster size and the strength or the thickness of the cara-pace. However, the lack of relationship is probably dueto the small range of sizes tested.

There was a significant positive relationship be-tween carapace thickness and strength for all 3 pointsin clawed lobsters (Fig. 6b, see Table 4 for all probabil-ities and r values). Among spiny lobsters, only PointBE showed a significant positive relationship betweencarapace thickness and strength (Table 4). There wasno significant relationship between carapace thicknessand strength for any of the 3 points among the slipperlobsters.

DISCUSSION

Predation

The striking outcome of these experiments was thatHomarus gammarus, with its massive claws, was themost vulnerable morphological type, while slipper lob-sters, which lack any morphological weapon, sufferedless predation than either of the other species of lob-ster. We demonstrated, however, that the claws areimportant weapons: without them, clawed lobsters aresimply bait, and have literally no chance of survival inthe open sea. Mortality of Palinura elephas was gener-ally intermediate between that of slipper and clawedlobsters. With their second antennae intact, spinylobsters suffered little mortality during the first 4 h ofpredator pressure, similar to slipper lobsters. Manipu-lated spiny lobsters suffered greater mortality thanintact spiny lobsters, but fared better than manipulatedclawed lobsters. In fact, the mortality of manipulated P.elephas was similar to that of intact H. gammarus.When shelter is at hand, the short-term effectiveness ofthe weapons of spiny and clawed lobsters could besufficient to allow them to escape from the predatorwith the abdominal tail-flip escape-response.

We were unable to demonstrate that clinging to thesubstrate was an effective antipredatory strategy for

slipper lobsters, as there was no significant differencebetween intact and manipulated individuals of thisspecies. Earlier experiments have indicated that ‘cling-ing’ by these lobsters is a vital part of their strategyagainst predation (Barshaw & Spanier 1994a,b). Theexplanation for this apparent discrepancy is simplythat in our experiment not enough slipper lobsterswere killed to allow us to test for differences betweenthe 2 treatments. In earlier experiments, slipper lob-sters were the only prey offered; consequently, therewas considerable predation upon them. In the presentexperiment, however, the predators preferentially killedthe other lobster species: out of the 40 slipper lobstersthat were tethered, only 3 were killed (1 intact and 2manipulated).

Increased exposure to predators decreased the effec-tiveness of the lobsters’ weapons. After 24 h there wasno longer a significant difference between intact andmanipulated clawed or spiny lobsters. Both strategiesof the fish (to bite off the eyes, and to bite at the clawsand antennae) rendered the weapons ineffective. After24 h, the intact lobsters actually had no functionalweapons: they had been ‘manipulated’ by the preda-tors themselves.

Tethering artifacts

The tethering technique we used in these experi-ments has potential artifacts that need to be under-stood and controlled (Peterson & Black 1994, Aronson& Heck 1995). We intentionally attracted predators toour site; thus, we did not measure the natural rate ofpredation, but instead measured the relative rate ofpredation on each treatment. What is important is thatthe act of tethering did not influence any one treatmentmore than another (Barshaw & Able 1990). For exam-ple, if the tether had made it difficult for clawed lob-sters to use their claws, but had had no effect on thearmor of slipper lobsters, that would have biased ourresults. However, we did extensive preliminary tether-ing tests, observing and videotaping the behavior ofthe different species while they were tethered in thefield, and ascertained that both spiny and clawed

lobsters were able to use their weaponswithout interference from their tethers.

There were indications that flight, par-ticularly explosive unpredictable flight(protean behavior), was a greater partof the antipredatory behavior of slipperlobsters than of the other species. Slipperlobsters are also known to be moreefficient swimmers that other lobsters(Spanier et al. 1991). Consequently itcould be that the slipper lobsters in our

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Table 4. Scyllarides latus, Palinurus elephas and Homarus gammarus. r andp-values for regressions on thickness of carapace versus force required tobreak carapace at 3 different points. Sl: slipper lobster; Sp: spiny lobster;

Cl: clawed lobster; ns: not significant

Species Back BE Side

Sl ns, r = 0.44 ns, r = 0.14 ns, r = 0.35

Sp ns, r = 0.24 p < 0.01, r = 0.63 ns, r = 0.23

Cl p < 0.04, r = 0.46 p < 0.03, r = 0.48 p < 0.001, r = 0.68

Barshaw et al.: Offense vs defense in lobsters

experiment were more affected by being tethered thanthe other 2 species. However, since slipper lobsterssuffered almost no predation, this possible artifactcannot have unduly biased our conclusions.

Other experimental artifacts

While the species we tested are sympatric over mostof their ranges (Fig. 1), the coast of Israel, where we didthese experiments, is home only to Scyllarides latus.Could it be that slipper lobsters are especially adaptedto the particular conditions in this area and for this rea-son they suffered less predation? The only predatorthroughout the experiment was the gray triggerfishBalistes carolinensis, which has a global distribution:it is found throughout the Mediterranean, with occa-sional occurrences in the Black Sea and on both sidesof the Atlantic from the North Sea to Angola and fromNova Scotia to Argentina (Lythgoe & Lythgoe 1992).Consequently, all 3 species of lobster have to contendwith triggerfish throughout their range. However, thefrequency with which the 3 species of lobster en-counter these triggerfish may not be equal. At presentthere are no publications on the predators or predationrates encountered by adult Homarus gammarus. Per-haps if clawed lobsters had more experience defend-ing themselves from triggerfish they would be lessvulnerable. We feel this would be an interesting topicfor further study.

Size

Body size affects the outcome of Predator-prey inter-actions across many taxa, including these species oflobsters, with greater size often providing a refugefrom predators (Eggleston et al. 1992). A small range ofsizes were used in the groups of slipper and clawedlobsters, and thus, no effects of size on predation ratewere detectable. In the spiny lobster group, however,there was a greater range of sizes, so it is not surprisingthat the larger intact spiny lobsters had a significantlygreater chance of surviving than smaller intact spinylobsters (Fig. 5). More interesting, perhaps, is that sizehad no effect on the survival of manipulated spinylobsters. It appears that larger weapons protect spinylobsters, not larger body size.

The fact that, in our experiment, spiny lobsters werelarger than slipper lobsters but were neverthelessmore vulnerable to predation, emphasizes the slipperlobsters’ defensive advantage. However, if the clawedlobsters in our experiment had been as large as thesespiny lobsters, perhaps the differences in vulnerabilitybetween them would have disappeared.

Carapace strength

The amount of predation suffered by the 3 species oflobsters was best explained by the strength of theirrespective carapaces, not by the weaponry they pos-sessed. Slipper lobsters suffered the least predationand had the strongest armor, spiny lobsters sufferedintermediate predation and had armor intermediate inboth strength and thickness, while clawed lobsterssuffered the greatest rates of predation and had theweakest armor. However, in the first 4 h of attack, theweapons of the spiny lobsters combined with theirarmor resulted in predation at the same low rate asslipper lobsters. It seems clear that increased strengthof armor increases the handling time for a predator to agreater extent than the possession of an offensiveweapon. Shell strength and resistance to breakageincreases as the third power of shell thickness (Wain-right et al. 1976, p. 256). Thus, slight increases in thick-ness should result in substantial increases in the forcerequired to break the shell, minimizing the effect ofincreased shell strength on the mobility of the lobster.In fact, slipper lobsters (with the strongest shell) swimfaster than either spiny or clawed lobsters (Spanier etal. 1991).

The strongest points on the carapace of slipper andspiny lobsters were Points Back and BE, which are thepoints most exposed during an attack by a fish. Itmakes sense for these 2 species of lobsters, which usearmor as protection against predation, to fortify themost vulnerable spots with the strongest armor. In con-trast, there was no difference between the strength ofthe 3 points on the carapace of the weak-shelledclawed lobsters, suggesting that the Homarus gam-marus exoskeleton is not modified as an antipredatormechanism against biting, crushing, or smashingpredators. Intraspecifically, only clawed lobsters showeda positive relationship between the thickness of thevarious points on their carapace and the strength orthose points.

Speculations

These data indicate that, at least for the suite of spe-cies we studied, passive, defensive antipredator strate-gies such as armor are more effective than active,offensive antipredator strategies such as weapons. Isdefense generally better than offense? We argue thatdefensive mechanisms may have general advantages.Weapons probably have a greater cost, as they requireenergy to grow and maintain, energy for vigilance tomonitor the position of the predator, energy to operateand, in the case of arthropods, may be autotomizedand require subsequent regeneration. Armor requires

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energy to grow (and of course with arthropods thearmor has to be re-grown after each molt) but, oncehardened, armor is a nonliving tissue that cannot besacrificed (as can appendages) and has no mainte-nance cost. It is interesting that, in contrast to Ver-meij (1987) who suggested that ‘hardening probablytakes longer for heavily armored arthropods’, weobserved that slipper lobsters hardened within 24 h ofmolting, while spiny lobsters took several days, andthin-shell clawed lobsters took many weeks or evenmonths to harden (D. E. Barshaw & K. L. Lavalli pers.obs.). Our observations are exactly what one wouldexpect if slipper lobsters rely on their armor and theother species do not.

Another advantage of defense is its passivity. If anantipredator mechanism does not require activity, itcould work better in concert with avoidance. Forexample, an organism relying on defence need notkeep its weapons between itself and the predator; itcan remain motionless even after it detects the preda-tor and may remain undetected longer. Also, morpho-logical weapons themselves could work against avoid-ance, as they could make an animal easier to detect(Dingle 1983).

Then why develop offensive capabilities? Whiledefensive antipredator characters evolve directly inresponse to predation, offensive antipredator charac-ters may evolve for multiple purposes, such as captur-ing food, defense of resources (food, shelter, territory),and obtaining mates (Dingle 1983). Thus, competingpressures may influence their design (Janzen 1981,Vermeij 1982) and they may not be optimized for any 1particular function. We have shown that the claws ofHomarus gammarus do indeed help protect it frompredation, so they are an antipredatory mechanism.However, their claws are also used in feeding as wellas in intraspecific competition for shelter and for mates(Lavalli & Factor 1995). The long antennae of spinylobsters have a sensory function, and a function inintraspecific competition (Zimmer-Faust et al. 1985).Therefore, it is probable that selection for large clawsor long antennae is not primarily the result of predationpressure. Defensive antipredator mechanisms, how-ever, develop directly in response to pressure frompredators and have no multiple-use constraints ontheir design. If there are compelling reasons other thanantipredator mechanisms for the evolution of weapons,why not have enhanced armor as well? Perhaps thisis the mechanism of spiny lobsters that have bothweapons and at least some protection from thicker,spinous armor. Of course, there are energy restraintson all organisms and trade-offs in design must bemade; thus, it might be impossible energetically tohave an organism with the claws of H. gammarus andthe armor of Scyllarides latus.

The species that we studied are sympatric over muchof their geographic distribution (Fig. 1), and are alsofound at similar depths and in similar habitats(Williams 1988, Holthuis 1991). However, the design ofanimals is affected not only by their environment(extrinsic factors), but also by ancestral, inherited limi-tations (intrinsic factors) that determine the directionsin which features can evolve (Lauder 1982). The scyl-larid and panulirid lobsters are temperate to subtropi-cal in their distribution, and first appeared in the lateTriassic. They diverged into many types, with the mod-ern slipper and spiny lobsters appearing in the lateJurassic (George & Mann 1968). Calcium carbonatedoes not precipitate as well in colder regions as it doesin warmer regions (Vermeij 1987), so perhaps part ofthe explanation for the heavy armor of the scyllaridline is that it evolved in warmer climates where armorwould not be as costly to manufacture.

Based on the many studies showing that competitionand predation rates are greater in lower latitudes(Schall & Pianka 1978, Vermeij 1987) it could be thattropical slipper and spiny lobsters experienced greaterpredation pressure which resulted in the evolution ofspecialized adaptations against predators, especiallyshell-breaking predators. Similarly, shell-breakingpredators have been cited as the evolutionary drivingforce behind the increased shell strength in gastropodsliving at lower latitudes (Vermeij 1987).

Nephropid lobsters (which include Homarus gam-marus) are all temperate to subarctic in distribution,and are relatively old and primitive, having divergedlittle from their first appearance in the Triassic (Glaess-ner 1969). We speculate that either (1) clawed lobstersbegan as and have remained a temperate species, withno impetus to evolve thicker shells, and have thus beenable to afford the energetic cost of large claws, or (2)they were competitively excluded from the lower lati-tudes due to some intrinsic factor such as the mainte-nance cost of large claws that precluded an evolution-ary increase in shell thickness.

Acknowledgements. We would like to thank our assistantsGuy Shakhaf and Amir Yurman for all of their help with lob-ster care and maintenance, diving, photography, and thelong hours they put in on these experiments in 1995 and1996. Stephen Breitstein, our dive operations officer, pro-vided invaluable assistance with tethering, videotaping, anddiving. Many others helped us with diving operations duringthe experiments, and we appreciate their efforts: Yossi Tur-Caspa, Avinoam Breitstein, Ronit Levy, Oz Goffman, Gre-gory Lavzin, and Tal Hershkovitz. We thank Donald Rich fororiginally suggesting a punch test as a way to measure thestrength of armor. We also thank him and Dr. Samuel Tarsi-tano of Southwest Texas State University for reviewing thismanuscript and for their many ideas and helpful discussions.We thank an anonymous reviewer who was unusually thor-ough and helpful, as well as Dr. Michael Childress, particu-

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larly for his statistical suggestions. Efrat Yaskil of the Univer-sity of Haifa was consulted on the MANOVA tests and pro-vided valuable information. We would also like to expressgratitude to Professor Tankum Weller, head of the MaterialsLaboratory in the Department of Engineering at the Tech-nion, Israel Institute for Technology in Haifa, Israel, for per-mission to use the MTS servo-controlled, hydraulic testingmachine. Ariel Greenwald, his technician, who helped usconduct the punch tests, is also acknowledged. Finally, wewould like to thank John Fouere of Cleggan Lobster Fish-eries and Christopher Kerrison of Colchester Oyster Fisheryfor their patience and help in fulfilling our rather odd lob-ster-purchase requests. During these experiments and thepreliminary runs in 1995, K.L.L. was supported by a US-Israel Fulbright Postdoctoral Award. This study was sup-ported by a grant from the Research Authority of HaifaUniversity.

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Editorial responsibility: Kenneth Heck (Contributing Editor), Dauphin Island, Alabama, USA

Submitted: April 18, 2002; Accepted: March 10, 2003Proofs received from author(s): June 23, 2003